Presynaptic facilitation of glutamate release in the basolateral amygdala: A mechanism for the anxiogenic and seizurogenic function of GluK1 receptors

Neuroscience

Volumn 221, Issue , 2012, Pages 157-169

  Aroniadou Anderjaska, V ^a   Pidoplichko, V I ^a   Figueiredo, T H ^a   Almeida Suhett, C P ^a   Prager, E M ^a   Braga, M F M ^a  

^a Uniformed Services University of the Health Sciences   (United States)

Author keywords

Anxiety; Basolateral amygdala; GluK1 kainate receptors; Presynaptic glutamate release; Seizures

Indexed keywords

1 (2 AMINO 2 CARBOXYETHYL) 3 (2 CARBOXYBENZYL)PYRIMIDINE 2,4 DIONE; 2 AMINO 3 (3 HYDROXY 5 TERT BUTYLISOXAZOL 4 YL)PROPANOIC ACID; GLUTAMIC ACID; KAINIC ACID RECEPTOR; KAINIC ACID RECEPTOR 1; KAINIC ACID RECEPTOR AGONIST; KAINIC ACID RECEPTOR ANTAGONIST; UBP 302; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY DISORDER; ARTICLE; BASOLATERAL AMYGDALA; BRAIN REGION; CONTROLLED STUDY; EVOKED CORTICAL RESPONSE; EXCITATORY POSTSYNAPTIC POTENTIAL; EXPERIMENTAL RAT; FACILITATION; GLUTAMATE RELEASE; IN VIVO STUDY; MALE; MINIATURE ENDPLATE POTENTIAL; NERVE CELL NETWORK; NEUROMODULATION; NEUROTRANSMITTER RELEASE; NONHUMAN; OPEN FIELD BEHAVIOR; PREPULSE INHIBITION; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; SEIZURE; STARTLE REFLEX; SYNAPTOSOME; TRANQUILIZING ACTIVITY;

ACOUSTIC STIMULATION; ALANINE; AMYGDALA; ANIMALS; BICUCULLINE; BIOPHYSICAL PHENOMENA; EXCITATORY AMINO ACID AGENTS; EXPLORATORY BEHAVIOR; GABA-A RECEPTOR ANTAGONISTS; GLUTAMIC ACID; MALE; MEMBRANE POTENTIALS; NEURONS; PATCH-CLAMP TECHNIQUES; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, KAINIC ACID; SENSORY GATING; SODIUM CHANNEL BLOCKERS; TETRODOTOXIN; THYMINE;

EID: 84864819631     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.07.006     Document Type: Article

References (72)

1. Alt A., Weiss B., Ogden A.M., Li X., Gleason S.D., Calligaro D.O., Bleakman D., Witkin J.M. In vitro and in vivo studies in rats with LY293558 suggest AMPA/kainate receptor blockade as a novel potential mechanism for the therapeutic treatment of anxiety disorders. Psychopharmacology (Berl) 2006, 185:240-247.
2. Alt A., Weiss B., Ornstein P.L., Gleason S.D., Bleakman D., Stratford R.E., Witkin J.M. Anxiolytic-like effects through a GLUK5 kainate receptor mechanism. Neuropharmacology 2007, 52:1482-1487.
3. Apland J.P., Aroniadou-Anderjaska V., Braga M.F. Soman induces ictogenesis in the amygdala and interictal activity in the hippocampus that are blocked by a GluR5 kainate receptor antagonist in vitro. Neuroscience 2009, 159:380-389.
4. Aroniadou-Anderjaska V., Qashu F., Maria Braga M.F. Mechanisms regulating gabaergic inhibitory transmission in the basolateral amygdala: implications for epilepsy and anxiety disorders. Amino Acids 2007, 32:305-315.
5. Aroniadou-Anderjaska V., Fritsch B., Qashu F., Braga M.F. Pathology and pathophysiology of the amygdala in epileptogenesis and epilepsy. Epilepsy Res 2008, 78:102-116.
6. Bettler B., Boulter J., Hermans-Borgmeyer I., O'Shea-Greenfield A., Deneris E.S., Moll C., Borgmeyer U., Hollmann M., Heinemann S. Cloning of a novel glutamate receptor subunit, GluR5: expression in the nervous system during development. Neuron 1990, 5:583-595.
7. Braga M.F., Aroniadou-Anderjaska V., Xie J., Li H. Bidirectional modulation of GABA release by presynaptic glutamate receptor 5 kainate receptors in the basolateral amygdala. J Neurosci 2003, 23:442-452.
8. A receptors on principal neurons. J Pharmacol Exp Ther 2009, 330:558-566.
9. Campbell S.L., Mathew S.S., Hablitz J.J. Pre- and postsynaptic effects of kainate on layer II/III pyramidal cells in rat neocortex. Neuropharmacology 2007, 53:37-47.
10. Chamberlain S.E., Jane D.E., Jones R.S. Pre- and post-synaptic functions of kainate receptors at glutamate and GABA synapses in the rat entorhinal cortex. Hippocampus 2012, 22:555-576.
11. Clarke V.R., Ballyk B.A., Hoo K.H., Mandelzys A., Pellizzari A., Bath C.P., Thomas J., Sharpe E.F., Davies C.H., Ornstein P.L., Schoepp D.D., Kamboj R.K., Collingridge G.L., Lodge D., Bleakman D. A hippocampal GluR5 kainate receptor regulating inhibitory synaptic transmission. Nature 1997, 389:599-603.
12. Clarke V.R., Collingridge G.L. Characterisation of the effects of ATPA, a GLU(K5) receptor selective agonist, on excitatory synaptic transmission in area CA1 of rat hippocampal slices. Neuropharmacology 2002, 42:889-902.
13. Clarke V.R., Collingridge G.L. Characterisation of the effects of ATPA, a GLU(K5) kainate receptor agonist, on GABAergic synaptic transmission in the CA1 region of rat hippocampal slices. Neuropharmacology 2004, 47:363-372.
14. Collingridge G.L., Olsen R.W., Peters J., Spedding M. A nomenclature for ligand-gated ion channels. Neuropharmacology 2009, 56:2-5.
15. Cossart R., Esclapez M., Hirsch J.C., Bernard C., Ben Ari Y. GluR5 kainate receptor activation in interneurons increases tonic inhibition of pyramidal cells. Nat Neurosci 1998, 1:470-478.
16. Davidson R.J., Abercrombie H., Nitschke J.B., Putnam K. Regional brain function, emotion and disorders of, emotion. Curr Opin Neurobiol 1999, 9:228-234.
17. Davis M., Rainnie D., Cassell M. Neurotransmission in the rat amygdala related to fear and anxiety. Trends Neurosci 1994, 17:208-214.
18. Debanne D., Guérineau N.C., Gähwiler B.H., Thompson S.M. Paired-pulse facilitation and depression at unitary synapses in rat hippocampus: quantal fluctuation affects subsequent release. J Physiol 1996, 491:163-176.
19. Etkin A., Wager T.D. Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. Am J Psychiatry 2007, 164:1476-1488.
20. Faraday M.M., Elliott B.M., Grunberg N.E. Adult vs. adolescent rats differ in biobehavioral responses to chronic nicotine administration. Pharmacol Biochem Behav 2001, 70:475-489.
21. Figueiredo T.H., Qashu F., Apland J.P., Aroniadou.-Anderjaska V., Souza A.P., Braga M.F. The GluR5 kainate/AMPA receptor antagonist LY293558 reduces soman-induced seizures and, neuropathology. J Pharmacol Exp Ther 2011, 336:303-312.
22. Fisahn A., Contractor A., Traub R.D., Buhl E.H., Heinemann S.F., McBain C.J. Distinct roles for the kainate receptor subunits GluR5 and GluR6 in kainate-induced hippocampal gamma oscillations. J Neurosci 2004, 24:9658-9668.
23. Fritsch B., Qashu F., Figueiredo T.H., Aroniadou-Anderjaska V., Rogawski M.A., Braga M.F. Pathological alterations in GABAergic interneurons and reduced tonic inhibition in the basolateral amygdala during epileptogenesis. Neuroscience 2009, 163:415-429.
24. Garrett A., Chang K. The role of the amygdala in bipolar disorder development. Dev Psychopathol 2008, 20:1285-1296.
25. Graham F.K. The more or less startling effects of weak prestimulation. Psychophysiology 1975, 12:238-248.
26. Gryder D.S., Rogawski M.A. Selective antagonism of GluR5 kainate receptor-mediated synaptic currents by topiramate in rat basolateral amygdala neurons. J Neurosci 2003, 23:7069-7074.
27. Handforth A., Ackermann R.F. Mapping of limbic seizure progressions utilizing the electrogenic status epilepticus model and the 14C-2-deoxyglucose method. Brain Res Brain Res Rev 1995, 20:1-23.
28. Hitchcock J.M., Davis M. Fear-potentiated startle using an auditory conditioned stimulus: effect of lesions of the amygdala. Physiol Behav 1987, 39:403-408.
29. Hoffman H.S., Ison J.R. Reflex modification in the domain of startle: I. Some empirical findings and their implications for how the nervous system processes sensory input. Psychol Rev 1980, 87:175-189.
30. Jane D.E., Lodge D., Collingridge G.L. Kainate receptors: pharmacology, function and therapeutic potential. Neuropharmacology 2009, 56:90-113.
31. Kaminski R.M., Banerjee M., Rogawski M.A. Topiramate selectively protects against seizures induced by ATPA, a GluR5 kainate receptor agonist. Neuropharmacology 2004, 46:1097-1104.
32. Khalilov I., Hirsch J., Cossart R., Ben-Ari Y. Paradoxical anti-epileptic effects of a GluR5 agonist of kainate receptors. J Neurophysiol 2002, 88:523-527.
33. Kotlinska J., Liljequist S. The putative AMPA receptor antagonist, LY326325, produces anxiolytic-like effects without altering locomotor activity in rats. Pharmacol Biochem Behav 1998, 60:119-124.
34. Kroner S., Rosenkranz J.A., Grace A.A., Barrionuevo G. Dopamine modulates excitability of basolateral amygdala neurons in vitro. J Neurophysiol 2005, 93:1598-1610.
35. Läck A.K., Diaz M.R., Chappell A., Dubois D.W., McCool B.A. Chronic ethanol and withdrawal differentially modulate pre- and post-synaptic function at glutamatergic synapses in rat basolateral amygdala. J Neurophysiol 2007, 98:3185-3196.
36. Läck A.K., Ariwodola O.J., Chappell A.M., Weiner J.L., McCool B.A. Ethanol inhibition of kainate receptor-mediated excitatory neurotransmission in the rat basolateral nucleus of the amygdala. Neuropharmacology 2008, 55:661-668.
37. Li H., Chen A., Xing G., Wei M.L., Rogawski M.A. Kainate receptor-mediated heterosynaptic facilitation in the amygdala. Nat Neurosci 2001, 4:612-620.
38. Li H., Rogawski M.A. GluR5 kainate receptor mediated synaptic transmission in rat basolateral amygdala in vitro. Neuropharmacology 1998, 37:1279-1286.
39. Li L., Fulton J.D., Yeomans J.S. Effects of bilateral electrical stimulation of the ventral pallidum on acoustic startle. Brain Res 1999, 836:164-172.
40. Li L., Du Y., Li N., Wu X., Wu Y. Top-down modulation of prepulse inhibition of the startle reflex in humans and rats. Neurosci Biobehav Rev 2009, 33:1157-1167.
41. McCool B.A., Chappell A. Strychnine and taurine modulation of amygdala-associated anxiety-like behavior is state-dependent. Behav Brain Res 2007, 178:70-81.
42. Menard J., Treit D. Effects of centrally administered anxiolytic compounds in animal models of anxiety. Neurosci Biobehav Rev 1999, 23:591-613.
43. Miyata M., Imoto K. Contrary roles of kainate receptors in transmitter release at corticothalamic synapses onto thalamic relay and reticular neurons. J Physiol 2009, 587:999-1012.
44. Mohapel P., Dufresne C., Kelly M.E., McIntyre D.C. Differential sensitivity of various temporal lobe structures in the rat to kindling and status epilepticus induction. Epilepsy Res 1996, 23:179-187.
45. More J.C., Nistico R., Dolman N.P., Clarke V.R., Alt A.J., Ogden A.M., Buelens F.P., Troop H.M., Kelland E.E., Pilato F., Bleakman D., Bortolotto Z.A., Collingridge G.L., Jane D.E. Characterisation of UBP296: a novel, potent and selective kainate receptor antagonist. Neuropharmacology 2004, 47:46-64.
46. Mulle C., Sailer A., Swanson G.T., Brana C., O'Gorman S., Bettler B., Heinemann S.F. Subunit composition of kainate receptors in hippocampal interneurons. Neuron 2000, 28:475-484.
47. Park K., Lee S., Kang S.J., Choi S., Shin K.S. Hyperpolarization-activated currents control the excitability of principal neurons in the basolateral amygdala. Biochem Biophys Res Commun 2007, 361:718-724.
48. B receptors. Neuropharmacology 2006, 51:1030-1037.
49. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1997, Academic Press, London.
50. Pitkanen A., Tuunanen J., Kalviainen R., Partanen K., Salmenpera T. Amygdala damage in experimental and human temporal lobe epilepsy. Epilepsy Res 1998, 32:233-253.
51. Prut L., Belzung C. The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur J Pharmacol 2003, 463:3-33.
52. Racine R.J. Modification of seizure activity by electrical stimulation: II. Motor Seizure. Electroencephalogr Clin Neurophysiol 1972, 32:281-294.
53. Racine R.J., Rose P.A., Burnham W.M. After discharge thresholds and kindling rates in dorsal and ventral hippocampus and dentate gyrus. Can J Neurol Sci 1977, 4:273-278.
54. Rainnie D.G., Asprodini E.K., Shinnick-Gallagher P. Intracellular recordings from morphologically identified neurons of the basolateral amygdala. J Neurophysiol 1993, 69:1350-1362.
55. Rodriguez-Moreno A., Lopez-Garcia J.C., Lerma J. Two populations of kainate receptors with separate signaling mechanisms in hippocampal interneurons. Proc Natl Acad Sci USA 2000, 97:1293-1298.
56. Rorick-Kehn L.M., Hart J.C., McKinzie D.L. Pharmacological characterization of stress-induced hyperthermia in DBA/2 mice using metabotropic and ionotropic glutamate receptor ligands. Psychopharmacology (Berl) 2005, 183:226-240.
57. Sanders S.K., Shekhar A. Regulation of anxiety by GABAA receptors in the ratamygdala. Pharmacol Biochem Behav 1995, 52:701-706.
58. Sang C.N., Hostetter M.P., Gracely R.H., Chappell A.S., Schoepp D.D., Lee G., Whitcup S., Caruso R., Max M.B. AMPA/kainate antagonist LY293558 reduces capsaicin-evoked hyperalgesia but not pain in normal skin in humans. Anesthesiology 1998, 89:1060-1067.
59. Sang C.N., Ramadan N.M., Wallihan R.G., Chappell A.S., Freitag F.G., Smith T.R., Silberstein S.D., Johnson K.W., Phebus L.A., Bleakman D., Ornstein P.L., Arnold B., Tepper S.J., Vandenhende F. LY293558, a novel AMPA/GluR5 antagonist, is efficacious and well-tolerated in acute migraine. Cephalalgia 2004, 24:596-602.
60. Smolders I., Bortolotto Z.A., Clarke V.R., Warre R., Khan G.M., O'Neill M.J., Ornstein P.L., Bleakman D., Ogden A., Weiss B., Stables J.P., Ho K.H., Ebinger G., Collingridge G.L., Lodge D., Michotte Y. Antagonists of GLU(K5)-containing kainate receptors prevent pilocarpine-induced limbic seizures. Nat Neurosci 2002, 5:796-804.
61. Stein M.B., Stein D.J. Social anxiety disorder. Lancet 2008, 371:1115-1125.
62. Sun H.Y., Bartley A.F., Dobrunz L.E. Calcium-permeable presynaptic kainate receptors involved in excitatory short-term facilitation onto somatostatin interneurons during natural stimulus patterns. J Neurophysiol 2009, 101:1043-1055.
63. Swerdlow N.R., Geyer M.A., Braff D.L. Neural circuit regulation of prepulse inhibition of startle in the rat, current knowledge and future challenges. Psychopharmacology 2001, 156:194-215.
64. Thomson A.M. Facilitation, augmentation and potentiation at central synapses. Trends Neurosci 2000, 23:305-312.
65. Vignes M., Clarke V.R.J., Parry M.C., Bleakman D., Lodge D., Ornstein P.L., Collingridge G.L. The GluR5 subtype of kainate receptor regulates excitatory synaptic transmission in areas CA1 and CA3 of the rat hippocampus. Neuropharmacology 1998, 37:1269-1277.
66. Washburn M.S., Moises H.C. Electrophysiological and morphological properties of rat basolateral amygdaloid neurons in vitro. J Neurosci 1992, 12:4066-4079.
67. White L.E., Price J.L. The functional anatomy of limbic status epilepticus in the rat. I. Patterns of 14C-2-deoxyglucose uptake and Fos immunocytochemistry. J Neurosci 1993, 13:4787-4809.
68. White L.E., Price J.L. The functional anatomy of limbic status epilepticus in the rat. II. The effects of focal deactivation. J Neurosci 1993, 13:4810-4830.
69. Womble M.D., Moises H.C. Hyperpolarization-activated currents in neurons of the rat basolateral amygdala. J Neurophysiol 1993, 70:2056-2065.
70. Wondolowski J., Frerking M. Subunit-dependent postsynaptic expression of kainate receptors on hippocampal interneurons in area CA1. J Neurosci 2009, 29:563-574.
71. Wu L.J., Ko S.W., Toyoda H., Zhao M.G., Xu H., Vadakkan K.I., Ren M., Knifed E., Shum F., Quan J., Zhang X.H., Zhuo M. Increased anxiety-like behavior and enhanced synaptic efficacy in the amygdala of GluR5 knockout mice. PLoS One 2007, 2:e167.
72. Wu L.J., Xu H., Ren M., Zhuo M. Genetic and pharmacological studies of GluR5 modulation of inhibitory synaptic transmission in the anterior cingulate cortex of adult mice. Dev Neurobiol 2007, 67:146-157.